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Bovine torovirus (Breda virus) revisited

Published online by Cambridge University Press:  28 February 2007

Armando E. Hoet*
Affiliation:
Facultad de Ciencias Veterinarias, La Universidad del Zulia, Maracaibo, Venezuela
Linda J. Saif
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, Ohio, USA
*
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Abstract

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Bovine torovirus (BoTV) is a pleomorphic virus with a spike-bearing envelope and a linear, non-segmented, positive-sense single-stranded RNA genome. This kidney-shaped virus is associated with diarrhea in calves and apparently has a worldwide distribution. This review provides details of the history and taxonomy of BoTV since its discovery in 1979. Information about virion morphology and architecture, antigenic and biological properties, viral genome, protein composition, thermal and chemical stability, and pH and proteolytic enzymes resistance is also summarized. A major focus of this review is to postulate a possible epidemiological cycle for BoTV, based on epidemiological data obtained in our studies and other published data, and progressing from the newborn calf to the adult animal. The distribution, host range, pathogenesis, disease and clinical signs (under experimental and natural exposure), pathology, diagnosis, prevention, treatment and control of BoTV infections are also described. In addition, a discussion of the zoonotic implications of torovirus-like particles detected in patients with gastroenteritis that resemble and cross-react with BoTV is presented. Hopefully, the findings described here will alert others to the existence of BoTV in cattle and its contribution to the diarrheal disease complex. This review also highlights the need for continual vigilance for potential zoonotic viruses belonging to the order Nidovirales, such as the SARS coronavirus.

Type
Research Article
Copyright
Copyright © CAB International 2004

References

Ali, A and Reynolds, DL (1997). Stunting syndrome in turkey poults: isolation and identification of the etiologic agent. Avian Diseases 41: 870881.CrossRefGoogle ScholarPubMed
Ali, A and Reynolds, DL (1998). The in vitro propagation of stunting syndrome agent. Avian Diseases 42: 657666.CrossRefGoogle ScholarPubMed
Ali, A and Reynolds, DL (2000). Characterization of the stunting syndrome agent: Relatedness to known viruses. Avian Diseases 44: 4550.CrossRefGoogle ScholarPubMed
Beards, GM, Green, J, Hall, C, Flewett, TH, Lamouliatte, F and du Pasquier, P (1984). An enveloped virus in stools of children and adults with gastroenteritis that resembles the Breda virus of calves. Lancet i: 10501052.Google Scholar
Beards, GM, Brown, DWG, Green, J and Flewett, TH (1986). Preliminary characterization of torovirus-like particles of humans: comparison with berne virus of horses and Breda virus of calves. Journal of Medical Virology 20: 6778.CrossRefGoogle ScholarPubMed
Boom, UVD (1986). Development of an ELISA for detecting toroviruses and torovirus antibodies in cattle; epidemiological studies on torovirus infections in cattle. Dissertation, Tierarztliche Hochschule, Hannover, German Federal Republic.Google Scholar
Bredenbeek, PJ, Snijder, EJ, Noten, AFH, den Boon, JA, Schaaper, WMM, Horzinek, MC and Spaan, WJM (1990). The polymerase gene of corona- and toroviruses: evidence for an evolutionary relationship. In: Cavanagh, D and Brown, TDK, editors. Coronaviruses and Their Diseases. New York: Plenum Press, pp. 307316.CrossRefGoogle Scholar
Brown, DWG, Beards, GM and Flewett, TH (1987). Detection of Breda virus antigen and antibody in humans and animals by enzyme immunoassay. Journal of Clinical Microbiology 25: 637640.Google Scholar
Brown, DWG, Selvakumar, R, Daniel, DJ and Mathan, VI (1988). Prevalence of neutralizing antibodies to Berne virus in animals and humans in Vellore, South India. Archives of Virology 98: 267269.CrossRefGoogle Scholar
Cavanagh, D (1997). Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Archives of Virology 143: 629633.Google Scholar
Cavanagh, D and Horzinek, MC (1993). Genus Torovirus assigned to the Coronaviridae. Archives of Virology 128: 395396.CrossRefGoogle Scholar
Cavanagh, D, Brian, DA, Enjuanes, L, Holmes, KV, Lai, MMC, Laude, H, Siddell, SG, Spaan, WJM, Taguchi, F and Talbot, PJ (1990). Recommendations of the Coronavirus Study Group for the Nomenclature of the Structural Proteins, mRNAs, and Genes of Coronaviruses. Virology 176, 306307.CrossRefGoogle Scholar
Cavanagh, D, Brian, DA, Brinton, MA, Enjuanes, L, Holmes, KV, Horzinek, MC, Lai, MMC, Laude, H, Plagemann, PGW, Siddell, SG, Spaan, WJM, Taguchi, F and Talbot, PJ (1994a). The Coronaviridae now comprises two genera, Coronavirus and Torovirus: report of the Coronaviridae study group. In: Laude, H and Vautherot, JF, editors. Coronaviruses: Molecular biology and Virus-Host Interactions. New York: Plenum Press, pp. 255257.CrossRefGoogle Scholar
Cavanagh, D, Brien, DA, Brinton, M, Enjuanes, L, Holmes, KV, Horzinek, MC, Lai, MMC, Laude, H, Plagemann, PGW, Spaan, WJM, Taguchi, F and Talbot, PJ (1994b). Revision of the taxonomy of the Coronavirus, Torovirus and Arterivirus genera. Archives of Virology 135: 227237.CrossRefGoogle ScholarPubMed
Chirnside, ED (1992). Equine arteritis virus: an overview. British Veterinary Journal 148: 181197.CrossRefGoogle ScholarPubMed
Cho, KJ, Hoet, AE, Loerch, SC, Wittum, TE and Saif, LJ (2001). Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattle. American Journal of Veterinary Research 62: 14361441.Google Scholar
Chouljenko, VN, Lin, XQ, Storz, J, Kousoulas, KG and Gorbalenya, AE (2001). Comparison of genomic and predicted amino acid sequences of respiratory and enteric bovine coronaviruses isolated from the same animal with fatal shipping pneumonia. Journal of General Virology 82: 29272933.CrossRefGoogle ScholarPubMed
Cornelissen, LAHM (1999). What are toroviruses? In: Cornelissen, LAHM, editor. Molecular Characterization of Ungulate Toroviruses. Utrecht: Universiteit Utrecht, pp. 720.Google Scholar
Cornelissen, LAHM, Wierda, CMH, Meer FJ van der, , Herrewegh, AAPM, Horzinek, MC, Egberink, HF and Groot, RJD (1997). Hemagglutinin–esterase, a novel structural protein of torovirus. Journal of Virology 71: 52275286.Google Scholar
Cornelissen, LAHM, van Woensel, PAM, de Groot, RJ, Horzinek, MC, Visser, N and Egberink, HF (1998). Cell culture-grown putative bovine respiratory torovirus identified as a coronavirus. Veterinary Record 142: 683686.Google Scholar
de Vries, AAF, Horzinek, MC, Rottier, PJM and de Groot, RJ (1997). The genome organization of the Nidovirales: similarities and differences between arteri-, toro-, and coronaviruses. Seminars in Virology 8, 3347.Google Scholar
Den Boon, JA, Snijder, EJ, Locker, JK, Horzinek, MC and Rottier, PJM (1991). Another triple-spanning envelope protein among intracellularly budding RNA viruses: the torovirus E protein. Virology 182: 655663.CrossRefGoogle ScholarPubMed
Draker, R, Tellier, R and Petric, M (2003). The complete genome sequence of the bovine torovirus: the first complete torovirus genome sequence [abstract]. In: 71st Conjoint Meeting of Canadian Association For Clinical Microbiology and Infectious Diseases, SP2. Montreal, Canada.Google Scholar
Duckmanton, LM, Luan, B, Devenish, J, Tellier, R and Petric, M (1997). Characterization of torovirus from human fecal specimens. Virology 239: 158168.Google Scholar
Duckmanton, LM, Carman, S, Nagy, E and Petric, M (1998a). Detection of bovine torovirus in fecal specimens of calves with diarrhea from Ontario farms. Journal of Clinical Microbiology 36: 12661270.Google Scholar
Duckmanton, LM, Tellier, R, Liu, P and Petric, M (1998b). Bovine torovirus: sequencing of the structural genes and expression of the nucleocapsid protein of Breda virus. Virus Research 58: 8396.CrossRefGoogle ScholarPubMed
Duckmanton, LM, Tellier, R, Richardson, C and Petric, M (1999). The novel hemagglutinin–esterase genes of humans torovirus and Breda virus. Virus Research 64: 137149.CrossRefGoogle ScholarPubMed
Durham, PJK, Hassard, LE, Norman, GR and Yemen, RL (1989). Viruses and virus-like particles detected during examination of feces from calves and piglets with diarrhea. Canadian Veterinary Journal 30: 876881.Google ScholarPubMed
Fagerland, JA, Pohlenz, JFL and Woode, GN (1986). A morphological study of the replication of breda virus (proposed family Toroviridae) in bovine intestinal cells. Journal of General Virology 67: 12931304.Google Scholar
Finlaison, DS (1995). Faecal viruses of dogs—an electron microscope study. Veterinary Microbiology 46: 295305.Google Scholar
Gonzalez, JM, Gomez-Puertas, P, Cavanagh, D, Gorbalenya, AE and Enjuanes, L (2003). A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Archives of Virology 148: 22072235.Google Scholar
Hall, GA (1987). Comparative pathology of infection by novel diarrhoea viruses. In: Brock, G and Whelan, J, editors. Novel Diarrhoea Viruses. Ciba Foundation Symposium No. 128. Chichester: John Wiley & Sons, pp. 192217.Google Scholar
Hasoksuz, MH, Lathrop, SL, Gadfield, KL and Saif, LJ (1999). Isolation of bovine respiratory coronaviruses from feedlot cattle and comparison of their biological and antigenic properties with bovine enteric coronaviruses. American Journal of Veterinary Research 60: 12271233.CrossRefGoogle ScholarPubMed
Heckert, RA, Saif, LJ, Hoblet, KH and Agnes, AG (1990). A longitudinal study of bovine coronavirus enteric and respiratory infections in dairy calves in two herds in Ohio. Veterinary Microbiology 22: 187201.Google Scholar
Heckert, RA, Saif, LJ and Myers, GW (1991a) Mucosal and systemic isotype specific antibody responses to bovine coronavirus structural proteins in naturally infected dairy calves. American Journal of Veterinary Research 52: 852857.CrossRefGoogle ScholarPubMed
Heckert, RA, Saif, LJ, Mengel, JP and Myers, GW (1991b) Mucosal and systemic antibody responses to bovine coronavirus structural proteins in experimentally challenge-exposed calves fed low or high amounts of colostral antibodies. American Journal of Veterinary Research 52: 700708.Google Scholar
Heckert, RA, Saif, LJ, Myers, GW and Agnes, AG (1991c). Epidemiologic factors and isotype-specific antibody responses in serum and mucosal secretions of dairy calves with bovine coronavirus respiratory tract and enteric tract infections. American Journal of Veterinary Research 52: 845851.Google Scholar
Hill, DL and Yang, T (1984). Virus-like particles in a positive case of canine parvovirus enteritis. Micron and Microscopica Acta 15: 207209.CrossRefGoogle Scholar
Hoet, AE (2002). Bovine torovirus (Breda virus): development of diagnostic tests and epidemiology. Thesis, Ohio State University, Columbus (OH).Google Scholar
Hoet, AE, Cho, KO, Chang, KO, Loerch, SC, Wittum, TE and Saif, LJ (2002). Enteric and nasal shedding of bovine torovirus (Breda virus) in feedlot cattle. American Journal of Veterinary Research 63: 342348.Google Scholar
Hoet, AE, Kyeong-Ok, C. and Saif, LJ (2003a). Comparison of ELISA and RT-PCR versus immune electron microscopy for detection of bovine torovirus (Breda virus) in calf fecal specimens. Journal of Veterinary Diagnostic Investigation 15: 100106.Google Scholar
Hoet, AE, Nielsen, PR, Hasoksuz, M, Thomas, C, Wittum, TE and Saif, LJ (2003b). Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. Journal of Veterinary Diagnostic Investigation 15: 205212.Google Scholar
Hoet, AE, Smiley, J, Thomas, C, Nielsen, PR, Wittum, TE and Saif, LJ (2003c). Association of enteric shedding of bovine torovirus (Breda virus) and other enteropathogens with diarrhea in veal calves. American Journal of Veterinary Research 64: 485490.Google Scholar
Holmes, KV (2001). Enteric infections with coronaviruses and toroviruses. Novartis Foundation Symposium 238: 258275.Google Scholar
Horzinek, MC (1993a). New virus diseases: visible evolution. Australian Veterinary Journal 70: 433436.Google Scholar
Horzinek, MC (1993b). Toroviruses—members of the coronavirus superfamily? Archives of Virology 7: 7580.Google Scholar
Horzinek, MC (1999). Toroviruses (Coronaviridae). In: Granoff, A and Webster, R, editors. Encyclopedia of Virology, 2nd edn. San Diego (CA): Academic Press, pp. 17981803.Google Scholar
Horzinek, MC and Weiss, M (1984). Toroviridae: a taxonomic proposal. Zentralblatt für Veterinärmedizin B 31: 649659.Google Scholar
Horzinek, MC and Weiss, M (1990). Toroviruses. In: Saif, LJ and Theil, KW, editors. Viral Diarrheas of Man and Animals. Boca Raton (FL): CRC Press, pp. 253262.Google Scholar
Horzinek, MC, Weiss, M and Ederveen, J (1984). Berne virus is not ‘Coronavirus-like’. Journal of General Virology 65: 645649.CrossRefGoogle Scholar
Horzinek, MC, Ederveen, J, Kaeffer, B, Boer de, D and Weiss, M (1986). The peplomers of Berne virus. Journal of General Virology 67: 24752483.CrossRefGoogle ScholarPubMed
Horzinek, MC, Weiss, M and Ederveen, J (1987a). Toroviridae: a proposed new family of enveloped RNA viruses. In: Brock, G and Whelan, J, editors. Novel Diarrhoea Viruses. Ciba Foundation Symposium, No. 128. Chichester: John Wiley & Sons, pp. 162174.Google Scholar
Horzinek, MC, Flewett, TH, Saif, LJ, Spaan, WJM, Weiss, M and Woode, GN (1987b). A new family of vertebrate viruses: Toroviridae. Intervirology 27: 1724.Google Scholar
Jamieson, FB, Wang, EEL, Bain, C, Good, J, Duckmanton, LM and Petric, M (1998). Human torovirus: a new nosocomial gastrointestinal pathogen. Journal of Infectious Diseases 178: 12631269.Google Scholar
Kaeffer, B, van Kooten, P, Ederveen, J, van Eden, W and Horzinek, MC (1989). Properties of monoclonal antibodies against Berne virus (Toroviridae). American Journal of Veterinary Research 50: 11311137.Google Scholar
Kapil, S and Goyal, SM (1995). Bovine coronavirus-associated respiratory disease. Compendium on Continuing Education for the Practicing Veterinarian 17: 11791181.Google Scholar
Kluver, S (1991). Electron microscopical and serological study of the occurrence of Breda torovirus, a cause of calf diarrhoea [abstract]. Tierarztliche Hochschule. Hannover, Germpany.Google Scholar
Koonin, EV (1991). The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. Journal of General Virology 72: 21972206.Google Scholar
Koopmans, M and Horzinek, MC (1994). Toroviruses of animals and humans: a review. Advances in Virus Research 43: 233273.Google Scholar
Koopmans, M and Horzinek, MC (1995). The pathogenesis of torovirus infections in animals and humans. In: Siddell, SG, editor. The Coronaviridae. New York: Plenum Press, pp. 403413.Google Scholar
Koopmans, M, Ederveen, J, Woode, GN and Horzinek, MC (1986). Surface proteins of Breda virus. American Journal of Veterinary Research 47: 18961900.Google ScholarPubMed
Koopmans, M, Van Den Boom, U, Woode, GN and Horzinek, MC (1989). Seroepidemiology of Breda Virus in Cattle using ELISA. Veterinary Microbiology 19: 233243.Google Scholar
Koopmans, M, Cremers, H, Woode, GN and Horzinek, MC (1990). Breda virus (Toroviridae) infection and systemic antibody response in sentinel calves. American Journal of Veterinary Research 51: 14431448.Google Scholar
Koopmans, M, Herrewegh, A and Horzinek, MC (1991a). Diagnosis of torovirus infection [letter]. Lancet 337: 859.Google Scholar
Koopmans, M, Snijder, EJ and Horzinek, MC (1991b). cDNA Probes for the Diagnosis of Bovine Torovirus (Breda Virus) Infection. Journal of Clinical Microbiology 29: 493497.Google Scholar
Koopmans, M, van Wuijckhuise-Sjouke, L, Schukken, YH, Cremers, H and Horzinek, MC (1991c). Association of diarrhea in cattle with torovirus infections on farms. American Journal of Veterinary Research 52: 17691773.Google Scholar
Koopmans, M, Monroe, SS, Coffield, LM and Zaki, SR (1993a). Optimization of extraction and PCR amplification of RNA extracts from paraffin-embedded tissue in different fixatives. Journal of Virology Methods 43: 189204.Google Scholar
Koopmans, M, Petric, M, Glass, RI and Monroe, SS (1993b). Enzyme-Linked Immunosorbent Assay Reactivity of Torovirus-Like Particles in Fecal Specimens from Humans with Diarrhea. Journal of Clinical Microbiology 31: 27382744.Google Scholar
Koopmans, M, Goosen, S, Lima, A, Mcauliffe, I, Nataro, J, Barret, L, Glass, RI and Guerrant, R (1997). Association of torovirus with acute and persistent diarrhea in children. Pediatric Infectious Disease Journal 16: 504507.Google Scholar
Krishnan, T and Naik, TN (1997). Electronmicroscopic evidence of torovirus like particles in children with diarrhoea. Indian Journal of Medical Research 105: 108110.Google Scholar
Kroneman, A, Cornelissen, LAHM, Horzinek, MC, Groot, RJD and Egberink, HF (1998). Identification and characterization of a porcine torovirus. Journal of Virology 72: 35073511.Google Scholar
Lacombe, D, Lamouliatte, F, Billeaud, C and Sandler, B (1988). Virus Breda et entéropathie hémorragique, Rappel á propos d'une observation. Archives Francaises de Pediatrie 45: 442.Google Scholar
Lamouliatte, F, du Pasquier, P, Rossi, F, Laporte, J and Loze, JP (1987). Studies on bovine Breda virus. Veterinary Microbiology 15: 261278.Google Scholar
Lathrop, SL, Wittum, TE, Brock, KV, Loerch, SC, Perino, LJ, Bingham, HR, McCollum, FT and Saif, LJ (2000). Association between infection of the respiratory tract attributed to bovine coronavirus and health and growth performance of cattle in feedlots. American Journal of Veterinary Research 61: 10621066.Google Scholar
Lavazza, A and Perini, S (1990). Su un episodio di diarrea nei suinetti, osservazione al microscopio elettronico di particelle torovirus-like (Electron microscopic visualization of porcine torovirus-like particles from gut contents of piglets). Atti della Societa Italiana Scientia Veterinaria 44: 765768.Google Scholar
Liebler, EM, Kluver, S, Pohlenz, JF and Koopmans, M (1992). The significance of bredavirus as a diarrhea agent in calf herds in Lower Saxony. Deutsche Tierärztliche Wochenschrift 99: 195200.Google Scholar
Lin, XQ, KL, OE, Storz, J, Purdy, CW and Loan, RW (2000). Antibody responses to respiratory coronavirus infections of cattle during shipping fever pathogenesis. Archives of Virology 145: 23352349.Google Scholar
Martin, SW, Nagy, E, Shewen, PE and Harland, RJ (1998). The association of titers to bovine coronavirus with treatment for bovine respiratory disease and weight gain in feedlot calves. Canadian Journal of Veterinary Research 62: 257261.Google Scholar
Matiz, K, Kecskeméti, S, Kiss, I, Adam, Z, Tanyi, J and Nagy, B (2002). Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. Acta Veterinaria Hungarica 50: 293296.Google Scholar
McNulty, MS, Bryson, DG, Allan, GM and Logan, EF (1984). Coronavirus infection of the bovine respiratory tract. Veterinary Microbiology 9: 425434.Google Scholar
Middleton, PJ (1996). Viruses that multiply in the gut and cause endemic and epidemic gastroenteritis. Clinical and Diagnostic Virology 6: 93101.Google Scholar
Muir, P, Harbour, DA, Gruffydd-Jones, TJ, Howard, PE, Hopper, CD, Gruffydd-Jones, EAD, Broadhead, HM, Clarke, CM and Jones, ME (1990). A clinical and microbiological study of cats with protruding nictitating membranes and diarrhoea: isolation of a novel virus. Veterinary Record 127: 324330.Google Scholar
Penrith, ML and Gerdes, GH (1992). Breda virus-like particles in pigs in South Africa. Journal of the South African Veterinary Association 63: 102.Google Scholar
Pérez, E, Kummeling, A, Janssen, MMH, Jiménez, C, Alvarado, R, Caballero, M, Donado, P and Dwinger, RH (1998). Infectious agents associated with diarrhoea of calves in the canton of Tilarán, Costa Rica. Preventive Veterinary Medicine 33: 195205.Google Scholar
Pohlenz, JF, Woode, GN, Cheville, NF, Mokresh, AH and Mohammed, KA (1982). Morphologic lesions in the intestinal mucosa of newborn calves reproduced by unclassified virus (‘Breda-virus’). In: Proceedings of XII World Congress of Cattle Disease 252–254Utrecht, Netherlands.Google Scholar
Pohlenz, JFL, Cheville, NF, Woode, GN and Mokresh, AH (1984). Cellular lesions in intestinal mucosa of gnotobiotic calves experimentally infected with a new unclassified bovine virus (Breda virus). Veterinary Pathology 21: 407417.Google Scholar
Pringle, CR (1992). Committee pursues medley of virus taxonomic issues. ASM News 58: 475476.Google Scholar
Reynolds, DJ, Debney, TG, Hall, GA, Thomas, LH and Parsons, KR (1985). Studies on the relationship between coronaviruses from the intestinal and respiratory tracts of calves. Archives of Virology 85: 7183.Google Scholar
Saif, LJ, Redman, DR, Theil, KW, Moorhead, PD and Smith, CK (1981). Studies on an enteric ‘breda’ virus in calves [abstract]. In: 62nd Annual Meeting Conference for Research Workers of Animal Diagnosis. 62: 42. Chicago, USA.Google Scholar
Saif, LJ, Redman, DR, Moorhead, PD and Theil, KW (1986). Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tract. American Journal of Veterinary Research 47: 14261432.Google Scholar
Scott, AC, Chaplin, MJ, Stack, MJ and Lund, LJ (1987). Porcine torovirus? Veterinary Record 120: 583.CrossRefGoogle ScholarPubMed
Scott, FMM, Holliman, A, Jones, GW, Gray, EW and Fitton, J (1996). Evidence of torovirus infection in diarrhoeic cattle. Veterinary Record 138: 284285.Google Scholar
Smith, DR, Fedorka-Cray, PJ, Mohan, R, Brock, KV, Wittum, TE, Morley, PS, Hoblet, KH and Saif, LJ (1998a). Epidemiologic herd-level assessment of causative agents and risk factors for winter dysentery in dairy cattle. American Journal of Veterinary Research 59: 9941001.Google Scholar
Smith, DR, Fedorka-Cray, PJ, Mohan, R, Brock, KV, Wittum, TE, Morley, PS, Hoblet, KH and Saif, LJ (1998b). Evaluation of cow-level risk factors for the development of winter dysentery in dairy cattle. American Journal of Veterinary Research 59: 986993.Google Scholar
Smiths, SL, Lavazza, A, Matiz, K, Horzinek, MC, Koopmans, MP and Groot, RJ (2003). Phylogenetic and evolutionary relationships among torovirus field variants: evidence for multiple intertypic recombination events. Journal of Virology 77: 95679577.Google Scholar
Snijder, EJ and Horzinek, MC (1993). Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. Journal of General Virology 74: 23052316.Google Scholar
Snijder, EJ and Horzinek, MC (1995). The molecular biology of toroviruses. In: Siddell, SG, editor. The Coronaviridae, New York: Plenum Press, pp. 219238.CrossRefGoogle Scholar
Snijder, EJ and Spaan, WJM (1995). The coronaviruslike superfamily. In: Siddell, SG, editor. The Coronaviridae, New York: Plenum Press, pp. 239255.CrossRefGoogle Scholar
Snijder, EJ, Ederveen, J, Spaan, WJM, Weiss, M and Horzinek, MC (1988). Characterization of Berne virus genomic and messenger RNAs. Journal of General Virology 69: 21352144.Google Scholar
Snijder, EJ, Boon, JAD, Spaan, WJM, Verjans, GMGM and Horzinek, MC (1989). Identification and primary structure of the gene encoding the Berne virus nucleocapsid protein. Journal of General Virology 70: 33633370.Google Scholar
Snijder, EJ, den Boon, JA, Bredenbeek, PJ, Horzinek, MC, Rijnbrand, R and Spaan, WJM (1990a). The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionary related. Nucleic Acids Research 18: 45354542.Google Scholar
Snijder, EJ, Boon, JAD, Spaan, WJM, Weiss, M and Horzinek, MC (1990b). Primary structure and post-translational processing of the Berne virus peplomer protein. Virology 178: 355363.CrossRefGoogle ScholarPubMed
Snijder, EJ, Horzinek, MC and Spaan, WJM (1990c). A 3'-coterminal nested set of independently transcribed mRNAs is generated during Berne virus replication. Journal of Virology 64: 331338.Google Scholar
Snijder, EJ, Horzinek, MC and Spaan, WJM (1994). The coronaviruslike superfamily. In: Laude, H and Vautherot, JF, editors. Coronaviruses: Molecular Biology and Virus–Host interactions. New York: Plenum Press, pp. 235244.Google Scholar
Spaan, WJM, Cavanagh, D and Horzinek, MC (1988). Coronaviruses: structure and genome expression. Journal of General Virology 69: 29392952.Google Scholar
Spaan, WJM, Boon, JAD, Bredenbeek, PJ, Hirnside, ED, Oten, AFH, Nijder, EJ, de Vries, AAF and Horzinek, MC (1990). Comparative and evolutionary aspects of coronaviral, arteriviral, and toroviral genome structure and expression. In: Brinton, MA and Heinz, FX, editors. New Aspects of Positive-strand RNA Viruses. Washington, DC: American Society for Microbiology, pp. 1219.Google Scholar
Storz, J, Stine, L, Liem, A and Anderson, GA (1996). Coronavirus isolation from nasal swap samples in cattle with signs of respiratory tract disease after shipping. Journal of the American Veterinary Medical Association 208: 14521455.Google Scholar
Storz, J, Lin-XiaoQing Purdy, CW, Chouljenko, VN, Kousoulas, KG, Enright, FM, Gilmore, WC, Briggs, RE and Loan, RW (2000a). Coronavirus and Pasteurella infections in bovine shipping fever pneumonia and Evans' criteria for causation. Journal of Clinical Microbiology 38: 32913297.Google Scholar
Storz, J, Purdy, CW, Lin-Xiao Qing, Burrell, M, Truax, RE, Briggs, RE, Frank, GH and Loan, RW (2000b). Isolation of respiratory bovine coronavirus, other cytocidal viruses, and Pasteurella spp from cattle involved in two natural outbreaks of shipping fever. Journal of the American Veterinary Medical Association 216: 15991604.Google Scholar
Tellier, R and Petric, M (1993). Human torovirus—purification from faeces [abstract]. In: IXth International Congress of Virology W24–4: 47.Google Scholar
Tzipori, S. (1985). The relative importance of enteric pathogens affecting neonates of domestic animals. In: Cornelius, CE and Simpson, CF, editors. Orlando (FL): Academic Press, pp. 103179.Google Scholar
Van Kruiningen, HJ, Castellano, VP, Koopmans, M and Harris, LL (1992). A serologic investigation for coronavirus and Breda virus antibody in winter dysentery of dairy cattle in the northeastern United States. Journal of Veterinary Diagnostic Investigation 4: 450452.CrossRefGoogle ScholarPubMed
Vanopdenbosch, E, Wellemans, G and Petroff, K (1991). Breda virus associated with respiratory disease in calves. Veterinary Record 129: 203Google Scholar
Vanopdenbosch, E, Wellemans, G, Charlier, G and Petroff, K (1992a). Bovine torovirus: cell culture propagation of a respiratory isolate and some epidemiological data. Vlaams Diergeneeskundig Tijdschrift 61: 4549.Google Scholar
Vanopdenbosch, E, Wellemans, G, Oudewater, J and Petroff, K (1992b). Prevalence of torovirus infections in Belgian cattle and their role in respiratory, digestive and reproductive disorders. Vlaams Diergeneeskundig Tijdschrift 61: 187191.Google Scholar
Vorster, JH and Gerdes, GH (1993). Breda virus-like particles in calves in South Africa. Journal of the South African Veterinary Association 64: 58Google Scholar
Ward, CW (1993). Progress towards a higher taxonomy of viruses. Research in Virology 144: 419453.Google Scholar
Weiss, M and Horzinek, MC (1986a). Resistance of Berne virus to physical and chemical treatment. Veterinary Microbiology 11: 4149.Google Scholar
Weiss, M and Horzinek, MC (1986b). Morphogenesis of Berne virus (proposed family Toroviridae). Journal of General Virology 67: 13051314.Google Scholar
Weiss, M and Horzinek, MC (1987). The proposed family Toroviridae: agents of enteric infections. Archives of Virology 92: 115.Google Scholar
Weiss, M, Steck, F and Horzinek, MC (1983). Purification and partial characterization of a new enveloped RNA virus (Berne virus). Journal of General Virology 64: 18491858.Google Scholar
Weiss, M, Steck, F, Kaderli, R and Horzinek, MC (1984). Antibodies to Berne virus in horses and other animals. Veterinary Microbiology 9: 523531.Google Scholar
Woode, GN (1982). Etiology of enteric viral infections of calves: pathological and clinical aspects. In: 12th World Congress on Cattle Diseases, pp. 201208. Utrecht, Netherlands.Google Scholar
Woode, GN (1987). Breda and Breda-like viruses: diagnosis, pathology and epidemiology. In: Brock, G and Whelan, J, editors. Novel Diarrhoea Viruses. Ciba Foundation Symposium, No. 128. Chichester: John Wiley & Sons, pp. 175191.Google Scholar
Woode, GN (1990). Breda virus. In: Dinter, Z and Morein, B, editors. Virus Infections of Ruminants. 3rd edn. Sweden: Elsevier Science, pp. 311316.Google Scholar
Woode, GN (1994). The toroviruses: bovine (Breda virus) and equine (Berne virus) and the torovirus-like agents of humans and animals. In: Kapikian, AZ, editor. Viral Infections of the Gastrointestinal Tract. 2nd edition. New York: Marcel Dekker, pp. 581602.Google Scholar
Woode, GN, Reed, DE, Runnels, PL, Herrig, MA and Hill, HT (1982). Studies with an unclassified virus isolated from diarrheic calves. Veterinary Microbiology 7: 221240.Google Scholar
Woode, GN, Mohammed, KA, Saif, LJ, Winand, NJ, Quesada, M, Kelso, NE and Pohlenz, JF (1983). Diagnostic methods for the newly discovered ‘Breda’ group of calf enteritis inducing viruses. In: Proceedings of the Third International Symposium of Veterinary Laboratory Diagnosticians, Volume 2, pp. 533538. Ames, USA.Google Scholar
Woode, GN, Pohlenz, JFL, Kelso-Gourley, NE and Fagerland, JA (1984). Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum. Journal of Clinical Microbiology 19: 623630.Google Scholar
Woode, GN, Saif, LJ, Quesada, M, Winand, NJ, Pohlenz, JFL and Gourley, NK (1985). Comparative studies on three isolates of Breda virus of calves. American Journal of Veterinary Research 46: 10031010.Google Scholar
Zanoni, R, Weiss, M and Peterhans, E (1986). The haemagglutinating activity of Berne virus. Journal of General Virology 67: 24852488.Google Scholar